Abstract
Elevated seawater pCO2, and in turn ocean acidification (OA), is now widely acknowledged to reduce calcification and growth of reef building corals. As with other environmental factors (e.g., temperature and nutrients), light availability fundamentally regulates calcification and is predicted to change for future reef environments alongside elevated pCO2 via altered physical processes (e.g., sea level rise and turbidity); however, any potential role of light in regulating the OA-induced reduction of calcification is still unknown. We employed a multifactorial growth experiment to determine how light intensity and pCO2 together modify calcification for model coral species from two key genera, Acropora horrida and Porites cylindrica, occupying similar ecological niches but with different physiologies. We show that elevated pCO2 (OA)-induced losses of calcification in the light (G L) but not darkness (G D) were greatest under low-light growth conditions, in particular for A. horrida. High-light growth conditions therefore dampened the impact of OA upon G L but not G D. Gross photosynthesis (P G) responded in a reciprocal manner to G L suggesting OA-relieved pCO2 limitation of P G under high-light growth conditions to effectively enhance G L. A multivariate analysis of past OA experiments was used to evaluate whether our test species responses were more widely applicable across their respective genera. Indeed, the light intensity for growth was identified as a significant factor influencing the OA-induced decline of calcification for species of Acropora but not Porites. Whereas low-light conditions can provide a refuge for hard corals from thermal and light stress, our study suggests that lower light availability will potentially increase the susceptibility of key coral species to OA.
References
Albright R, Mason B, Miller M, Langdon C (2012) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci USA 107:20400–20404
Al Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426
Allemand D, Tambutté É, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (Eds.) Coral reefs: an ecosystem in transition. Springer Inc., pp 119–150
Anthony KRN, Kline DI, Diaz-Pulido S, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446
Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471
Barnes DJ (1982) Light response curve for calcification in the staghorn coral Acropora acuminata. Comp Biochem Physiol A 73:41–45
Brading P, Davey P, Smith DJ, Achterberg A, Warner ME, Suggett DJ (2011) Differential impact of ocean acidification amongst phylotypes of Symbiodinium. Limnol Oceanogr 56:927–938
Bucher DJ, Harriott VJ, Roberts LG (1998) Skeletal micro-density, porosity and bulk density of acroporid corals. J Exp Mar Biol Ecol 228:117–136
Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res Oceans 110: doi: 10.1029/2004JC002671
Chan NCS, Connolly S (2012) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Global Change Biol. doi:10.1111/gcb.12011
Colombo-Palotta MF, Rodriguez-Roman A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907
Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol 16:851–863
De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119
Dunne RP, Brown BE (2001) The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs 20:201–210
du Putron SJ, McCorkle DC, Cohen AL, Dillon AB (2010) The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs 30:321–328
Edmunds PJ (2011) Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56:2402–2410
Edmunds PJ (2012) Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea. French Polynesia. Mar Biol 159:2149–2160
Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea. French Polynesia. Global Change Biol. doi:10.1111/j.1365-2486.2012.02695.x
Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457
Gatusso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: A review on interactions and control by carbonate chemistry. Am Zool 39:160–183
Hennige SJ, Walsh SJ, McGinly M, Smith DJ, Warner ME, Suggett DJ (2010) Coral acclimation and adaptation along an environmental gradient of an Indonesian reef complex. J Exp Mar Biol Ecol 391:143–152
Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98
Hii YS, Bolong AMA, Yang TT, Liew HC (2009) Effect of elevated carbon dioxide on two scleractinian corals: Porites cylindrica (Dana, 1846) and Galaxea fascicularis (Linnaeus, 1767) J. Mar Biol. doi:10.1155/2009/215196
Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 238:1523–1528
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Holcomb M, Cohen AL, McCorkle DC (2012) An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9:29–39
Intergovernmental Panel on Climate Change (2007) Climate change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge Univ Press, New York
Jokiel PL (2011) Ocean acidification and control of reef coral calcification by boundary layer limitation of proton flux. Bull Mar Sci 87:639–657
Jury CP, Whitehead RF, Szmant AM (2010) Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells, 1973): bicarbonate concentrations best predict calcification rates. Global Change Biol 16:1632–1644
Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159
Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110 doi: 10.1029/2004JC002576
Langdon C, Taakhashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson MJ (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cycles 14:639–645
Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377
Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations, ORNL/ CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, TN
Marubini F, Barnett H, Langdon C, Atkinson MJ (2001) Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Mar Ecol Prog Ser 220:153–162
Marubini F, Ferrier-Pages C, Furla P, Allemand D (2008) Coral calcification responds to seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs 27:491–499
McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Climate Change. doi:10.1038/NCLIMATE1473
Moya A, Tambutte S, Bertucci A, Tambutte E, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D (2008) Carbonic anhydrase in the coral Stylophora pistillata: characterization, localization and role in biomineralization. J Biol Chem 283:25475–25484
Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition I. δ13C of zooxanthellae and animal tissue versus depth. Mar Biol 100:185–193
Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Predicting coral reef futures under global warming and ocean acidification. Science 333:418–422
Ries JB, Cohen AL, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674
Rodolfo-Metalpa R, Houlbrèque F, Tambutté E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso JP, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 1:308–312
Roy RN, Roy LN, Vogel KM, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45 °C. Mar Chem 4:249–267
Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371
Smith S, Kinsey D (1978) Calcification and organic carbon metabolism as indicated by carbon dioxide. In: Stoddart D, Johannes R (eds) Coral reefs: Research methods. Monographs on oceanographic methodology, UNESCO, Paris, pp 469–484
West JM, Salm RV (2003) Resistance and resilience to coral bleaching: Implications for coral reef conservation and management. Conserv Biol 19:956–967
Wild C, Hoegh-Guldberg BO, Naumann MS, Colombo-Pallotta MF, Ateweberhan M, Fitt WK, Iglesias-Prieto R, Palmer C, Bythell JC, Ortiz JC, Loya Y, van Woesik R (2011) Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar Freshw Res 62:205–215
Yentsch CS, Yentsch CM, Cullen JJ, Lapointe B, Phinney DA, Yentsch SW (2002) Sunlight and water transparency: cornerstones in coral research. J Exp Mar Biol Ecol 268:171–183
Acknowledgments
We are extremely grateful to two anonymous reviewers and to Neil Chan and Sean Connolly (ICRS, Cairns 2012) for their insightful comments that helped to improve upon an earlier version of the manuscript, and also, to Mr. Russell Smart and Ms. Sarah Jane-Walsh for support in maintaining coral acclimation tanks and monitoring seawater chemistry. Funding was provided by the National Environmental Research Council UK (NERC grant NE/G020116/1). Author contributions: DJSu, TL and DJSm conceived the study and wrote the paper; LD and TL constructed the CO2-stat facility, and (with LT) produced and analyzed experimental data; EL and DJSu collated and analysed the meta-data set.
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Suggett, D.J., Dong, L.F., Lawson, T. et al. Light availability determines susceptibility of reef building corals to ocean acidification. Coral Reefs 32, 327–337 (2013). https://doi.org/10.1007/s00338-012-0996-7
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DOI: https://doi.org/10.1007/s00338-012-0996-7